Perinatology.  2018 Sep;29(3):114-120. 10.14734/PN.2018.29.3.114.

Maternal Smoke during Pregnancy Programs for Bone Disturbance in Offspring

• Cho GJ
• Sim JY
• Kim SE
• Hong HR
• Ahn KH
• Hong SC
• Oh MJ
• Kim HJ

• KMID: 2421576
• DOI: http://doi.org/10.14734/PN.2018.29.3.114

Abstract

OBJECTIVE
A number of epidemiological studies have reported that smoking causes a decrease in bone mineral density (BMD) and an increase in the risk of bone fracture, and is a risk factor for osteoporosis. Maternal smoking during pregnancy results in a variety of adverse developmental outcomes associated with intrauterine growth restriction. However, little is known about the effect of maternal smoking during pregnancy on BMD in the offspring.
METHODS
Pregnant CD-1 mice were exposed to cigarette smoke (1 or 2 cigarettes/day, 5 days/week) (smoke group) or sham exposed (control group) throughout pregnancy. After delivery, nursing dams and offspring were kept together in individual cages. At 4 weeks, the fourth lumbar vertebral body of each offspring was scanned with a micro- computed tomography apparatus. Trabecular parameters including bone volume fraction (bone volume/total volume, %), thickness (mm), number (1/mm), and separation (mm) were evaluated. The BMD was also measured.
RESULTS
No differences in the trabecular bone volume fraction, thickness, separation, and number and the BMD were observed between the offspring of the control and 1 cigarette smoking dams. However, trabecular bone volume fraction, thickness, number, and the BMD were significantly lower, whereas trabecular separation was higher in the offspring of 2 cigarette smoking dams compared with those of the offspring from control dams.
CONCLUSION
Maternal smoking during pregnancy decreased BMD and altered bone microarchitecture in the offspring. These results will become a great source to inform the importance of quitting smoking during pregnancy.

Keyword

Bone; Cigarette; Pregnancy; Mice

MeSH Terms

Animals
Bone Density
Epidemiologic Studies
Fractures, Bone
Mice
Nursing
Osteoporosis
Pregnancy*
Risk Factors
Smoke*
Smoking
Tobacco Products
Smoke

Figure

• 

  Fig. 1 The characteristics of the bone mineral density (BMD) of the fourth lumbar vertebral body from the control, 1 cigarette, and 2 cigarette groups (n=8 for each group). *P<0.05.

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  Fig. 2 Representative 2-dimensional (A–F) and 3-dimensional (G–I) micro-computed tomography images of the fourth lumbar vertebral body from the control (A, D, G), 1 cigarette (B, E, H), and 2 cigarette (C, F, I) groups.

• 

  Fig. 3 The characteristics of the microarchitecture of the fourth lumbar vertebral body from the control, 1 cigarette, and 2 cigarette groups (n=8 for each group). Bone volume fraction (A), trabecular thickness (B), number (C) and separation (D). *P<0.05.

• 

  Fig. 4 The biochemical characteristics of bone turnover in the control, 1 cigarette, and 2 cigarette groups (n=8 for each group). CTX, C-terminal telopeptides of type I collagen. OC, osteocalcin. *P<0.05.

Reference

1. Hodgson TA. Cigarette smoking and lifetime medical expenditures. Milbank Q. 1992; 70:81–125.

2. Tsevat J. Impact and cost-effectiveness of smoking interventions. Am J Med. 1992; 93:43S–47S.

3. Daniell HW. Osteoporosis of the slender smoker. Vertebral compression fractures and loss of metacarpal cortex in relation to postmenopausal cigarette smoking and lack of obesity. Arch Intern Med. 1976; 136:298–304.

4. Hopper JL, Seeman E. The bone density of female twins discordant for tobacco use. N Engl J Med. 1994; 330:387–392.

5. Krall EA, Dawson-Hughes B. Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res. 1999; 14:215–220.

6. Tong VT, Dietz PM, Morrow B, D'Angelo DV, Farr SL, Rockhill KM, et al. Trends in smoking before, during, and after pregnancy--Pregnancy Risk Assessment Monitoring System, United States, 40 sites, 2000-2010. MMWR Surveill Summ. 2013; 62:1–19.

7. Jhun HJ, Seo HG, Lee DH, Sung MW, Kang YD, Syn HC, et al. Self-reported smoking and urinary cotinine levels among pregnant women in Korea and factors associated with smoking during pregnancy. J Korean Med Sci. 2010; 25:752–757.

8. Cnattingius S. The epidemiology of smoking during pregnancy: smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine Tob Res. 2004; 6:Suppl 2. S125–S140.

9. Godfrey K, Walker-Bone K, Robinson S, Taylor P, Shore S, Wheeler T, et al. Neonatal bone mass: influence of parental birthweight, maternal smoking, body composition, and activity during pregnancy. J Bone Miner Res. 2001; 16:1694–1703.

10. Jones G, Riley M, Dwyer T. Maternal smoking during pregnancy, growth, and bone mass in prepubertal children. J Bone Miner Res. 1999; 14:146–151.

11. Venkataraman PS, Duke JC. Bone mineral content of healthy, full-term neonates. Effect of race, gender, and maternal cigarette smoking. Am J Dis Child. 1991; 145:1310–1312.

12. Beamer WG, Shultz KL, Donahue LR, Churchill GA, Sen S, Wergedal JR, et al. Quantitative trait loci for femoral and lumbar vertebral bone mineral density in C57BL/6J and C3H/HeJ inbred strains of mice. J Bone Miner Res. 2001; 16:1195–1206.

13. Rodrigues AM, Caetano-Lopes J, Vale AC, Aleixo I, Pena AS, Faustino A, et al. Smoking is a predictor of worse trabecular mechanical performance in hip fragility fracture patients. J Bone Miner Metab. 2012; 30:692–699.

14. Schuit SC, van der Klift M, Weel AE, de Laet CE, Burger H, Seeman E, et al. Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam Study. Bone. 2004; 34:195–202.

15. Bouxsein ML, Karasik D. Bone geometry and skeletal fragility. Curr Osteoporos Rep. 2006; 4:49–56.

16. Grampp S, Lang P, Jergas M, Glüer CC, Mathur A, Engelke K, et al. Assessment of the skeletal status by peripheral quantitative computed tomography of the forearm: short-term precision in vivo and comparison to dual X-ray absorptiometry. J Bone Miner Res. 1995; 10:1566–1576.

17. Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, et al. Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res. 2000; 15:13–19.

18. Akhter MP, Lund AD, Gairola CG. Bone biomechanical property deterioration due to tobacco smoke exposure. Calcif Tissue Int. 2005; 77:319–326.

19. Ma D, Li Y, Hackfort B, Zhao Y, Xiao J, Swanson PC, et al. Smoke-induced signal molecules in bone marrow cells from altered low-density lipoprotein receptor-related protein 5 mice. J Proteome Res. 2012; 11:3548–3560.

20. Gao SG, Li KH, Xu M, Jiang W, Shen H, Luo W, et al. Bone turnover in passive smoking female rat: relationships to change in bone mineral density. BMC Musculoskelet Disord. 2011; 12:131.

21. Yoon V, Maalouf NM, Sakhaee K. The effects of smoking on bone metabolism. Osteoporos Int. 2012; 23:2081–2092.

22. Heinz-Erian P, Spitzmüller A, Schröcksnadel H, Birnbacher R. Maternal smoking and inhibition of fetal growth factor. JAMA. 1998; 279:1954.

23. Haste FM, Brooke OG, Anderson HR, Bland JM. The effect of nutritional intake on outcome of pregnancy in smokers and non-smokers. Br J Nutr. 1991; 65:347–354.

24. D'Souza SW, Black P, Richards B. Smoking in pregnancy: associations with skinfold thickness, maternal weight gain, and fetal size at birth. Br Med J (Clin Res Ed). 1981; 282:1661–1663.

25. Bush PG, Mayhew TM, Abramovich DR, Aggett PJ, Burke MD, Page KR. A quantitative study on the effects of maternal smoking on placental morphology and cadmium concentration. Placenta. 2000; 21:247–256.

26. Cooper C, Westlake S, Harvey N, Javaid K, Dennison E, Hanson M. Review: developmental origins of osteoporotic fracture. Osteoporos Int. 2006; 17:337–347.

27. Hovi P, Andersson S, Järvenpää AL, Eriksson JG, Strang-Karlsson S, Kajantie E, et al. Decreased bone mineral density in adults born with very low birth weight: a cohort study. PLoS Med. 2009; 6:e1000135.

28. Beltrand J, Alison M, Nicolescu R, Verkauskiene R, Deghmoun S, Sibony O, et al. Bone mineral content at birth is determined both by birth weight and fetal growth pattern. Pediatr Res. 2008; 64:86–90.

29. Gale CR, Martyn CN, Kellingray S, Eastell R, Cooper C. Intrauterine programming of adult body composition. J Clin Endocrinol Metab. 2001; 86:267–272.

30. Martínez-Mesa J, Restrepo-Méndez MC, González DA, Wehrmeister FC, Horta BL, Domingues MR, et al. Life-course evidence of birth weight effects on bone mass: systematic review and meta-analysis. Osteoporos Int. 2013; 24:7–18.

31. Colak O, Alataş O, AydoXğdu S, Uslu S. The effect of smoking on bone metabolism: maternal and cord blood bone marker levels. Clin Biochem. 2002; 35:247–250.

32. Fang MA, Frost PJ, Iida-Klein A, Hahn TJ. Effects of nicotine on cellular function in UMR 106-01 osteoblast-like cells. Bone. 1991; 12:283–286.

33. Rothem DE, Rothem L, Soudry M, Dahan A, Eliakim R. Nicotine modulates bone metabolism-associated gene expression in osteoblast cells. J Bone Miner Metab. 2009; 27:555–561.

34. Beamer WG, Donahue LR, Rosen CJ, Baylink DJ. Genetic variability in adult bone density among inbred strains of mice. Bone. 1996; 18:397–403.